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Somatosensation in Social Perception

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Somatosensation in Social Perception REVIEWS Somatosensation in social perception Christian Keysers*‡, Jon H. Kaas§ and Valeria Gazzola*‡ Abstract | The discovery of mirror neurons in motor areas of the brain has led many to assume that our ability to understand other people’s behaviour partially relies on vicarious activations of motor cortices. This Review focuses the limelight of social neuroscience on a different set of brain regions: the somatosensory cortices. These have anatomical connections that enable them to have a role in visual and auditory social perception. Studies that measure brain activity while participants witness the sensations, actions and somatic pain of others consistently show vicarious activation in the somatosensory cortices. Neuroscientists are starting to understand how the brain adds a somatosensory dimension to our perception of other people. Vicarious activation One of the most exciting developments of the past expressions such as “Her words were really touch- Activation of a brain region that decade is the discovery that our perception of other ing” encapsulate the intuitive link between the people is normally involved in individuals involves neurons and brain areas that were around us and our sense of touch. processing the observer’s own thought to be reserved for the control of our own In this Review, we first describe the location and con- actions and sensations, but (FIG. 1) that is now activated by seeing actions and the experience of our own emotions. First, nections of the somatosensory cortices to show similar actions or sensations in it became clear that seeing or hearing other people’s that, in contrast to the early somatosensory cortices in another person. actions recruits neurons1–8 (in monkeys) and brain the central sulcus, all other somatosensory cortices regions (in humans) in the premotor and posterior (where the later stages of somatosensory processing Proprioception parietal cortices that are also involved in programming take place) receive direct input from areas known to The sense through which we 9–18 perceive the position and similar actions . This has led to the idea that under- have visual and auditory properties. Second, we show movements of our own body. standing the inner state of other individuals relies on that in agreement with this anatomical evidence, the implicit motor simulation — that is, the activation of higher stages of somatosensory processing in the pri- motor programs that we would use to perform similar mary somatosensory cortex (SI) and secondary soma- actions19–23. Our motor cortices seemed no longer ‘pri- tosensory cortex (SII) are activated when we perceive *Social Brain Laboratory, vate’ but a part of our social brain, processing the states other people being touched, performing an action or Department of Neuroscience, of others as if they were our own. experiencing somatic pain (BOX 1). We suggest that these University Medical Center More recently, it has been suggested that brain areas vicarious activations of somatosensory cortices may have Groningen, A. Deusinglaan 2, 9713AW Groningen, involved in emotion processing, including the anterior the unique potential to provide a somatic dimension to The Netherlands. insula and the rostral cingulate cortex (rCC), might our perception of other people’s experiences. ‡Social Brain Laboratory, perform an ‘emotional simulation’ of other individuals’ Netherlands Institute for experiences, showing activity not only when we expe- Anatomy of the somatosensory system Neuroscience, Royal rience positive and negative emotions but also when Somatosensation involves the processing of tactile, Netherlands Academy of Arts 24–45 proprioceptive nociceptive and Sciences (KNAW), we witness those of others . Electrostimulation and information. Here, we Meibergdreef 47, 1105BA of similar regions of the insula causes measurable briefly describe the cortical regions involved in this Amsterdam, The Netherlands. changes in the body (for example, gastric contrac- processing and examine which of these brain regions §Department of Psychology, tions) and induces the perception of changes in the receive the visual and auditory information that would Vanderbilt University, PMB 46 (FIG. 1) 407817, 2301 Vanderbilt body . This suggests that emotional simulation is be necessary to trigger vicarious responses . Place, Nashville, Tennessee not purely conceptual but involves representations of Traditionally, in humans and monkeys the term ‘som- 37240-7817 USA. the body. Current models of social cognition there- atosensory cortices’ refers to the anterior parietal cortex Correspondence to C.K. fore incorporate the notion that motor and emotional and the upper bank (operculum) of the lateral sulcus, and V.G. e-mails: brain regions can contribute to our perception of oth- which process tactile, proprioceptive and nociceptive [email protected]; [email protected] ers by simulating other people’s actions and emotions. information. The term ‘somatosensory system’ refers to doi:10.1038/nrn2833 The somatosensory cortices have so far been ignored all of the brain regions involved in processing somato- Published online 6 May 2010 by mainstream simulation models19,20,23. However, sensory information, and includes the somatosensory NATURE REVIEWS | NEUROSCIENCE VOLUME 11 | JUNE 2010 | 417 © 2010 Macmillan Publishers Limited. All rights reserved REVIEWS a rCC CS c PCS BA2 PF, PFG and VIP M1 ex BA BA BA BA ex rt 3a 3b 1 2 rt co co 1 PM VIP PM M1 BA BA3b SII PF BA3a PFG rCC culum S Oper ST Insula Lateral Visual sulcus cortex (opened) Thalamus Insula Thalamus STS Auditory cortex ain stem Br b CS PCS No vicarious Strong vicarious M1 BA1BA2 BOLD responses BOLD responses BA3b BA3a Figure 1 | Cortical processing networks for somatosensation. a | Posteriolateral view ofNa a humanture Re viebrainws |showing Neuroscienc arease and regions involved in somatosensation. The central sulcus (CS), posterior central sulcus (PCS) and lateral sulcus have been opened to show the areas within. The superior temporal sulcus (STS) is not opened, but it contains multisensory areas on its banks. Other sulci are not shown. For clarity, the rostral cingulate cortex (rCC) is indicated on the medial wall of the opposite hemisphere. The anterior parietal cortex includes the four strip-like areas of Brodmann area 3a (BA3a), BA3b, BA1 and BA2 (shown in green) in a rostrocaudal sequence. Regions of interest in the posterior parietal cortex include the ventral intraparietal area (VIP) and more lateral regions (PF and PFG). The lateral parietal cortex is inside the lateral sulcus. It includes the operculum of the upper bank, which contains the secondary somatosensory cortex (SII, composed of the secondary somatosensory cortex proper (S2) and the parietal ventral region (PV)), and the insula, which has regions for processing touch and pain. Somatosensory networks ultimately involve the primary motor (M1) cortex and the dorsal and ventral premotor (PM) areas for action. The thalamus (dashed grey lines) lies deep in the forebrain. b | Schematic representation of the CS, the PCS, the M1 cortex and the anterior parietal areas BA3a, BA3b, BA1 and BA2. c | Brain regions involved in somatosensation, their main connections and their source of visual input. Functional MRI experiments suggest that vicarious activation occurs in some somatosensory brain regions; the strength of the blood oxygen level-dependent (BOLD) response in these regions to observing the touch, actions or pain of others is indicated by the colour. In addition, there are brain regions with neurons that respond to the presentation of visual or auditory stimuli that also show vicarious activation; these are the PM, STS and areas PF, PFG and VIP (shown in blue). cortices proper plus the insula and the rostral cingulate + BA2 when it is unclear to which of these subregions a cortex, which are thought to process the affective value statement applies or when it applies to all four. of somatosensory stimuli47. BA3a receives proprioceptive information, largely The anterior parietal cortex consists of four parallel, from muscle spindle receptors through the ventropos- mediolateral strips of cortex: the classical cytoarchitec- terior superior nucleus (VPS) of the thalamus, and has Nociception tonic areas 3a, 3b, 1 and 2 of Brodmann and the Vogts. close anatomical connections with the motor cortex. The sense through which we In humans, Brodmann area 3 (BA3a and BA3b) roughly BA3b is the primary area for tactile processing and perceive damage caused to our correspond to the posterior bank of the central sulcus, receives its major activating inputs from neurons in the own body — for example, by excessive heat, cold or BA1 to the crown of the postcentral gyrus and BA2 to ventroposterior nucleus (VP) of the thalamus. BA3b physical injury. the anterior bank of the postcentral gyrus (FIG. 1a,b). All also receives input from small neurons in the VP and four areas were once considered to be parts of a single in the ventroposterior inferior nucleus (VPI) that are Muscle spindle receptors ‘homunculus’, a systematic representation of the contra- activated by a broad range of stimulation intensities Receptors in the muscles that lateral body surface known as ‘SI’. It is now known that (including touch in the nociceptive range) and from measure changes in muscle 48 length and hence changes in each of the four areas constitutes a separate representation nociceptive neurons in the spinal cord and brain stem . 47 the location of the relevant with different connections and functions
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